Recent developments and innovations in solid state fermentation

+Model

ARTICLE IN PRESS

BIORI-2; No. of Pages 20

Biotechnology Research and Innovation (2017) xxx, xxx---xxx

http://www.journals.elsevier.com/biotechnology-research-and-innovation/

REVIEW ARTICLE

Recent developments and innovations in solid state fermentation Carlos Ricardo Soccol ∗ , Eduardo Scopel Ferreira da Costa, Luiz Alberto Junior Letti, Susan Grace Karp, Adenise Lorenci Woiciechowski, Luciana Porto de Souza Vandenberghe Bioprocess Engineering and Biotechnology Department, Federal University of Paraná (UFPR), 81531-970 BR-Curitiba, PR, Brazil Received 16 November 2016; accepted 10 January 2017

KEYWORDS Solid-state fermentation; Bioreactors; Patents; Agro-industrial substrates

Abstract After forty years of research development, an overview of solid-state fermentation (SSF), focusing on its applications, mainly of the very recent papers of the last five years, is presented. This review comprises the most important developed processes concerning the production of enzymes, biopulping processes, and traditional processes, for food fermentation, such as the production of Chinese daqu and koji, and industrial important biomolecules such as organic acids, pigments, phenolic compounds, aromas and biosorbents. SSF bioreactors design that has been developed is reported, so as the solutions for the classical drawbacks and the most important cases of successful employment of the technique are described. And, finally, it is summarized a very interesting report of patents and innovations regarding SSF products and processes. © 2017 Sociedade Brasileira de Biotecnologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/4.0/).

Introduction Solid state fermentation (SSF) is a process in which microorganisms grow in an environment without free water, or with very low content of free water. Its historical importance for humankind date from thousands of years ago, mainly for food processing, both in western (bread and cheese) and eastern (Koji) countries. Considering the last century and the recent decades it is still used for production of important

∗

Corresponding author. E-mail: [email protected] (C.R. Soccol).

biomolecules and products for many industries, including food, pharmaceutical, textile, biochemical and bioenergy, among others (Pandey, 2003; Soccol & Vandenberghe, 2003). The main counterpart for SSF is the submerged fermentation (Smf), a process in which microorganisms grow in liquid medium, with high content of free water. Biological processes carried out in Smf have notable advantages regarding instrumentation and control (monitoring of pH, dissolved oxygen, temperature, concentration of water soluble molecules), separation of biomass after the fermentation, mixing, aeration and scaling up (Farinas, 2015). Contrarily, SSF mimics the natural habitat of most part of microorganisms (mainly fungi and mold); demand less

http://dx.doi.org/10.1016/j.biori.2017.01.002 2452-0721/© 2017 Sociedade Brasileira de Biotecnologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

2

C.R. Soccol et al.

energy for sterilization (because of lower water activity); is less susceptible to bacterial contamination; regarding the products, it enables higher enzymatic productivity for many enzymes, it is less susceptible to substrate inhibition, and hence it allows higher final concentration of products; has several environmental advantages, since it allows the use of solid agro-industrial wastes as substrate and/or energy source in their natural form and facilitates the solid waste management, besides lesser wastewater production (Singhania, Patel, Soccol, & Pandey, 2009). Other aspects cited as positive concerning SSF are: the higher quality and higher activity of extracts; no need of organic solvents (which generally confer some level of toxicity for the extract); lower capital and operating costs; reduced downstream processing and reduced stirring (Martins et al., 2011; Singhania et al., 2009). Considering historical aspects, the perspectives, and also taking into account the high density of papers about SSF, this article aims to present an overview of the subject including the main applications, of the last five years, and an interesting summary of patents and innovations developed in the area.

Microorganisms The most important factors to be considered during the development of a SSF are the choice of microorganisms and the choice of substrates. Microorganisms that are particularly suitable for SSF are the filamentous fungi, since the technique simulates their natural habitat. In this condition, they are able to synthesize considerable amounts of enzymes and other metabolites (Farinas, 2015). Although filamentous fungi are considered the most appropriate microorganisms for SSF, and secondly the yeasts, which are also able to grow in a low water activity environment, there are also some species of bacteria (e.g. Bacillus subtilis, Bacillus thuringiensis and Lactobacillus sp.) which have been reported to successfully produce enzymes in solidstate condition (Singhania et al., 2009). Actinomycetes such as Streptomyces sp. are also indicated for SSF processes since they present characteristics such as abundant colonization of solid residues, production of a wide range of degradative enzymes and high resistance to extreme conditions (Orozco et al., 2008).

Substrates The most promising residues for SSF include agricultural and forestry residues, which are very abundant and normally underutilized. A fraction is used to generate electricity, while another large fraction that is burned without energy recovery or remains in the field, representing an environmental problem (Farinas, 2015). Agro residues that can be used as substrates for SSF include sugarcane bagasse, cassava bagasse, cereal brans such as wheat bran, rice bran, oat bran and soybean bran, coffee pulp and husks, fruit peels and pulps, corn cobs, straws and husks of different origins. These materials are basically composed by cellulose, hemicellulose, lignin, starch, pectin and other fibers (Farinas, 2015; Singhania et al., 2009; Soccol & Vandenberghe, 2003).

The choice of the most appropriate microorganisms to be cultivated in the agro residue depends much on its composition. In the case of lignocellulosic residues, the wood rotting fungi are usually the most indicated. Wood rotting fungi can be classified in white-rot fungi (Basidiomycetes and some Ascomycetes), which preferentially degrade lignin, brownrot fungi (Basidiomycetes), which degrade cellulose and hemicelluloses, and the soft-rot fungi (e.g. Aspergillus niger and Trichoderma reesei), which secrete a complete system of cellulases (Yoon, Ang, Ngoh, & Chua, 2014). Usually, these agro residues are not only a solid support for nutrients absorption and biomass growth, but they are also a source of carbon and nutrients. Sometimes, supplementation is needed in order to provide all necessary nutrients for optimum growth. Macro and micronutrients that are usually added to the medium include phosphorus, sulfur, potassium, magnesium, calcium, zinc, manganese, copper, iron, cobalt, and iodine (Farinas, 2015; Pandey, 2003; Soccol & Vandenberghe, 2003). Cost and availability are the main factors to be considered in the choice of a residue as substrate or support in SSF. However, other characteristics such as crystallinity, accessible area, surface area, porosity, and particle size are important aspects to be considered for SSF process (Farinas, 2015; Singhania et al., 2009).

Applications of SSF Enzymes The majority of SSF scientific papers, which were published in the last five years, are related to enzyme production, mainly cellulases and xylanases production. The class of the cellulases is formed by endoglucanases (EC 3.2.1.4) that cleave randomly the cellulose chain, exoglucanases (EC 3.2.1.74 and EC 3.2.1.91), which catalyze the hydrolysis of chain ends, and ␤-glucosidases (EC 3.2.1.21), also called cellobiases, that hydrolyse the product of the exoglucanases releasing glucose monomers (Kuhad et al., 2016). Xylanases are a class of enzymes that catalyze the hydrolysis of 1,4␣-D-xylosidic linkages in xylans, one of the components of the hemicellulose fraction of plant cell walls. Carboxy methyl cellulase (CMCase) activities between 172 U/g and 545 U/g were obtained, which represents the activity of endoglucanases, produced from substrates such as wheat bran, corn stover and apple pomace by filamentous fungi (A. niger, Aspergillus fumigatus and Rhyzopus oryzae). For xylanase, activities as high as 73,000 U/g or 98,000 U/g were reported, this time by Bacillus species cultivated on wheat bran (Table 1). Both classes of enzymes have important applications in the conversion of biomass to products such as ethanol, and also other important applications in the textile, paper, food and beverages industries. Proteases were the third most studied group of enzymes produced by SSF in the recent literature. They were produced from various agro industrial and also from tannery industry wastes, especially by fungi of the genus Aspergillus. Activities higher than 3000 U/g and higher than 50,000 U/g were reported (Table 1). Proteases are considered the most significant industrial enzymes, representing around 60% of the global market, with applications in detergents,

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Substrate/support

Productivity

Bioreactor

Reference

Bacillus licheniformis AT70

Date waste

209 U/g, 7 days

Flasks

Wheat straw Apple pomace

6900 U/g, 5 days 3309 U/g, 120 h

Flasks Flasks

Amylase Amylase

Bacillus sp. BBXS-2 Macrophomina phaseolina Aspergillus oryzae Thermomyces sp.

Wheat bran Soy and bread waste

1491 U/g, 3 days 39,900 U/g, 4 days

Flasks 4.5 L cylindrical reactor

Amylase Cellulase Cellulase

Aspergillus oryzae S2 Rhizopus oryzae SN5 Aspergillus fumigatus

Starch and soybean meal Wheat bran Corn stover

Flasks Flasks Flasks

Cellulase

Aspergillus niger NRRL 2001

Apple pomace, rice husk and lactoserum

Cellulase

Aspergillus niger NRRL-567

Apple pomace

Cellulase

Aspergillus niger NS-2

Wheat bran

Laccase

Brewer’s spent grain

Laccase Laccase

Trametes versicolor ATCC 20869 Pleurotus ostreatus Pleurotus sp.

22,118 U/g, 12 days 437 U/g, 5 days 526 U/g (CMCase), 145 U/g (FPase), 4 days 401 U/g (FPase), 545 U/g (CMCase), 285 U/g (␤-glucosidase), 96 h 134 U/g (Fpase), 60 U/g (␤-glucosidase), 172 U/g (CMCase), 48 h 395 U/g (CMCase), 28 U/g (FPase), 46 U/g (␤-glucosidase), 96 h 13,506 U/g, 12 days

Afrisham, Badoei-Dalfard, Namaki-Shoushtari, and Karami (2016) Qureshi et al. (2016) Kaur, Dhillon, Brar, and Chauhan (2012) Chen et al. (2014) Cerda, El-Bakry, Gea, and Sánchez (2016) Sahnoun et al. (2015) Pandey, Edgard, and Negi (2016) Liu et al. (2011)

Sugarcane bagasse Coconut coir

Laccase

Pleurotus ostreatus

Laccase

Enzymes Amylase

Amylase Amylase

Laccase Laccase

Lipase Lipase

Tray-type

Dhillon, Brar, Kaur, Metahni, and M’hamdi (2012)

Flasks

Dhillon, Kaur, Brar, and Verma (2012)

Flasks

Bansal, Tewari, Soni, and Soni (2012)

Tray-type

Dhillon, Kaur, and Brar (2012)

167 U/g, 5 days 54,600 U/g, 8 days

Flasks Tray-type

Wheat bran

32,450 U/g, 7 days

Flasks

Pyrenophora phaeocomes Coriolus sp.

Rice straw

10,859 U/g, 4 days

Flasks

Wheat bran

2661 U/g, 10 days

Flasks

Ganoderma lucidum and Saccharomyces cerevisiae Penicillium simplicissimum Pseudomonas aeruginosa PseA

Glucose

38,000 U/L, 8 days

Castor bean waste

155 U/g, 96 h

Biomembrane-surface liquid co-culture (BSLCc), 100 L Tray-type

Karp et al. (2012) Bhattacharya, Garlapati, and Banerjee (2011) El-Batal, ElKenawy, Yassin, and Amin (2015) Rastogi, Soni, Kaur, and Soni (2016) Mathur, Mathur, Sharma, and Chauhan (2013) Hailei, Chaozhi, Guangli, and Ping (2013)

Deoiled Jatropha curcas seed cake

932 U/g, max. 9 days

Flasks

Godoy, Gutarra, Castro, Machado, and Freire (2011) Joshi, Mathur, and Khare (2011)

ARTICLE IN PRESS

Microorganism

+Model

Product

BIORI-2; No. of Pages 20

Reports of enzyme production in SSF in the last 5 years.

Recent developments and innovations in solid state fermentation

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Table 1

3

Product

Substrate/support

Productivity

Bioreactor

Reference

Burkholderia cenocepacia Schizophyllum commune ISTL04 Thermomucor indicae seudaticae N31 Aspergillus oryzae CPQBA 394-12 DRM 01 Aspergillus niger F3

Sugarcane bagasse, sunflower seed and olive oil Leucaena leucocephala seeds Sugarcane bagasse and soybean oil Citrus pulp and sugarcane bagasse Citrus peel

72.3 U/g, 96 h

Flask

Liu, Li, Meng, and Yan (2016)

146.5 U/g, 5 days

Flasks

15 U/g, 72 h

Polypropylene bags

Singh, Singh, Kumar, and Thakur (2014) Ferrarezi et al. (2014)

40 U/g, 18---24 h

Pilot scale packed-bed

Biz et al. (2016)

265 U/g, 96 h

Horizontal drum

Static flasks

52230 U/g, 14 days (336 h)

10-L air tight reactors (batch fermentation)

Yazid, Barrena, and Sánchez (2016)

Protease

Aspergillus niger LBA 02

262.78 U/g, 48 h

Static flasks

Castro et al. (2015)

Protease

Aspergillus oryzae CCBP 001

Chickling vetchpeels/grass pea peels (CVP) Hair wastes from the tannery industry as substrate and anaerobically digested sludge as co-substrate Wheat bran, soybean meal, cotton seed meal and orange peel Canola cake

5266.8 U/mL, 96 h

Protease

Aspergillus terreus NCFT 4269.10 Consortium

Rodríguez-Fernández, Rodríguez-León, Carvalho, Sturm, and Soccol (2011) Sethi et al. (2016)

From 355.5 U/g before spray drying. Activity of 1388.25 (after spray drying)

Freitas et al. (2015)

Protease

Aspergillus versicolor CJS-98 Aspergillus oryzae

Jatropha seed cake

3366 U/g, 96 h

Laboratory scale system consisting of 16 columns (2.5 cm diameter, 20 cm length) placed in a water bath Static flasks

Screw-pressed Jatropha curcas seed

3094 U/g, 96 h

Static flasks

Protease and glucoamylase Protease

Aspergillus awamori

Waste bread

9 cm Petri dishes

Pleurotus sajor-caju

Static flasks

Ravikumar, Gomathi, Kalaiselvi, and Uma (2012)

Xylanase

Trichoderma viride-IR05

Wheat bran, rice bran, green gram, corn flour and ragi Wheat bran, rice polish, rice husk, soybean meal, sunflower meal, sugarcane bagasse and corn cobs

102.8 U/g (glucoamylase), 63.7 U/g (protease), 168 h Around 85 U/mL, 192 h

72.4 U/g, 168 h

Static flasks

Irfan, Nadeem, and Syed (2014)

Lipase Lipase Lipase Pectinase Pectinase

Protease

Protease

ARTICLE IN PRESS

Microorganism

+Model

(Continued)

BIORI-2; No. of Pages 20

4 Veerabhadrappa, Shivakumar, and Devappa (2014) Thanapimmetha, Luadsongkram, Titapiwatanakun, and Srinophakun (2012) Melikoglu, Lin, and Webb (2013)

C.R. Soccol et al.

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Table 1

Substrate/support

Productivity

Bioreactor

Reference

Sorghum straw

5177.23 U/g, 120 h

Static flasks

Xylanase

Aspergillus tubingensis FDHN1 Bacillus sp. PKD-9

Wheat bran

98000 U/g, 120 h

Static flasks

Xylanase

Bacillus aerophilus KGJ2

45.9 U/g, 24 h

Static flasks

Xylanase, CMCase, FPase and B-glucosidase

Aspergillus fumigatus SK1

Wheat bran, tea dust, sawdust, paper waste, cassava bagasse, rice straw and rice husk Untreated oil palm trunk

Adhyaru, Bhatt, Modi, and Divecha (2016) Panwar, Srivastava, and Kapoor (2014) Gowdhaman et al. (2014)

Static flasks

Ang, Shaza, Adibah, Suraini, and Madihah (2013)

Xylanase

Aspergillus oryzae (P6B2)

Wheat bran

54.27 U/g (CMCase), 3.36 U/g (FPase), 4.54 U/g (␤-glucosidase), 418.70 U/g (xylanase), 96 h 2830.7 IU/g, 24 h

Pirota et al. (2013)

Xylanase and cellulase

Aspergillus niger FGSCA733

Jatropha curcas seed cake

Lab-scale system consisting of 16 columns (2.5 cm diameter, 20 cm length) placed in a water bath Static flasks

Xylanase

Promicromonospora sp. MARS Bacillus pumilus

Rice straw

Aluminum trays (5 cm × 2.5 cm × 2 cm) Not informed

Kumar, Joshi, Kashyap, and Khanna (2011) Kapilan and Arasaratnam (2011)

437.54 U/g (cellulase) and 273.83 U/g (xylanase), 120 h 158.4 U/g, 96 h

Static flasks

Pandey et al. (2016)

Static flasks

Kaushik, Mishra, and Malik (2014)

73,000 U/g, 48 h 770 U/g, 72 h 176 U/g, 196 h. After ion exchange chromatography 2560 U/g of protein

Static flasks Static flasks Static flasks

Nagar et al. (2011) Garai and Kumar (2013) Chanwicha, Katekaew, Aimi, and Boonlue (2015)

Xylanase

Xylanase

Xylanase and cellulase Xylanase

Rhizopus oryzae SN5

Xylanase Xylanase Xylanase

Bacillus pumilus SV-85S Aspergillus candidus Thermoascus aurantiacus var. levisporus KKU-PN-I2-1

Aspergillus lentulus

Paddy husk (support); corncob as C source; groundnut powder or sesame seedcake powder or coconut seedcake powder or soy meal powder as N source Wheat bran Wheat bran, corn cob, sugarcane bagasse and wheat straw Wheat bran Wheat bran Sugarcane bagasse and rice bran (1:1, w/w)

6087 U/g and 3974 U/g of xylanase (48 h) and cellulose (120 h) respectively 85.0 IU/g, 96 h 326.5 U/g, 144 h

Ncube, Howard, Abotsi, Jansen van Rensburg, and Ncube (2012)

YP/S , product yield from substrate (g g−1 ).

ARTICLE IN PRESS

Microorganism

+Model

Product

BIORI-2; No. of Pages 20

(Continued)

Recent developments and innovations in solid state fermentation

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Table 1

5

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

6

C.R. Soccol et al.

leather processing, food and feed processing, pharmaceuticals, chemicals and waste treatment (Sethi, Jana, Nanda, Mohapatrac, & Sahoo, 2016). Laccases (benzenediol:oxygen oxidoreductase, EC 1.10.3.2), which are polyphenol oxidases that find many applications in biopulping, biobleaching, detoxification of environmental pollutants, pharmaceuticals, preparation of beverages, among others (Dhillon, Kaur, & Brar, 2012), were produced from agro wastes such as sugarcane bagasse, wheat bran, rice straw, and brewer’s spent grain. The highest reported activity was obtained with coconut coir fermented by Pleurotus sp. (54,600 U/g in 8 days, according to Table 1). Lipases (triacylglycerol lipase, E.C. 3.1.1.3) were also produced from oily residues or fibrous residues enriched with oil, using both fungi (Penicillium simplicissimum, Schizophyllum commune, Thermomucor indicae seudaticae) and bacteria (Pseudomonas aeruginosa, Burkholderia cenocepacia), and activities between 15 U/g and 932 U/g were reported (Table 1). Applications of lipases include detergents, synthesis of pharmaceuticals, cosmetics, food processing, textile processing and, more recently, the synthesis of biodiesel (Ferrarezi et al., 2014). Finally, amylases (E.C. 3.2.1.) were produced from residues such as wheat bran and straw, apple pomace, soy, bread and date waste, some of them enriched with starch, and different microorganisms were employed (Aspergillus oryzae, Bacillus spp., Thermomyces sp. and Macrophomina phaseolina). Highest activity (39,900 U/g in 4 days, Table 1) was obtained with soy and bread waste fermented by Thermomyces sp. Amylases are widely employed in the food industry, for ethanol production from starchy materials, and in pharmaceuticals, paper and detergents, representing around 30% of the global market of enzymes (Singh & Gupta, 2014).

Biopulping Biopulping is a kind of biomass pretreatment that promotes the delignification of cellulosic material through the action of ligninolitic exoenzymes produced ‘‘in situ’’, which is normally performed by fungi that grow onto the solid ligninolitic material or a solid process fermentation. These enzymes act on the solid substrate, breaking the chemical bonds of the lignin molecule, depolymerizing the whole structure into smaller structures (Mendonc ¸a, Guerra, & Ferraz, 2002). The fungus must be selected according its enzymatic activities, presenting a high laccase and peroxidase activity and a low cellulasic activity to preserve the cellulosic fraction. This leads to preferably digestion of the lignin that is present in the vegetable cell wall. Due to the mild conditions used, biopulping produces cellulose pulp demanding less energy and chemical products in a less severe process compared to the chemical or mechanical conventional pulping. Also, biopulping improves the cellulose recovering yield and the quality of the paper fiber (Fonseca et al., 2014). The most common and efficient fungi used are those of the wood decomposition, known as the white rot fungi and the brown rot fungi, that during their secondary metabolism secret these enzymes (Fernández-Fernández, Sanromán, & Moldes, 2013). Trametes e Pleurotus genus

are the most studied such as Trametes pubescens (Galhaup, Goller, Peterbauer, Strauss, & Haltrich, 2002), Trametes versicolor (Font, Caminal, Gabarrell, Romero, & Vicent, 2003), Trametes hirsuta (Rodríguez-Couto & Toca-Herrera, 2006), Pleurotus ostreatus (Lenz---Hölker, 2004), but it can also be cited Coriolus hirsutus (Koroleva et al., 2002), Pycnoporus cinnabarinus (Meza, Auria, Lomascolo, Sigoillot, & Casalot, 2007), Neurospora crassa (Cabana, Jones, & Agathos, 2007; Luke & Burton, 2001). The disadvantage of the biopulping is the time demanding for the process including time necessary to the fungus growth and the substrate colonization, so an alternative to turn the process faster is the application of the enzymatic ligninolitic ‘‘pool’’, produced in an optimized fermentative process. This enzymatic pretreatment was proposed as an alternative to the biological pretreatments that use the fungus application onto the material to be treated, slower due to the time demanding to the fungus growth and the difficulties to keep the process aseptic for long time periods (Martín-Sampedro, Eugenio, & Villar, 2012). The enzymatic pulping besides replacing the fungus direct application and reducing the time necessary to the process, can also replace the chemical catalysts of the traditional thermochemical pulping, promoting the material’s digestion in milder conditions. The production of the ligninolitic enzymatic pool is carried out in bioreactors under controlled and optimized conditions. The enzymatic broth produced can be composed by the desired enzymes according to the material to be treated and the fraction of the material is supposed to be preserved (Hyeon et al., 2014).

Starters in oriental and western countries Many products employ ‘‘starter cultures’’ which are cultivated in SSF. These starter cultures are usually considered as one of the ingredients to prepare a broad set of products, such as liquors, vinegars, rice wines (e.g. the very well known sake), soy sauce (e.g. shoyu), distilled beverages (e.g. shochu), meat sauce and soybean paste (e.g. miso), among others. In western countries, it is usual to name all these starter cultures as koji, but in truth there are specific classifications, such as the Chinese qus (daqu, Xiaoqu, Hongqu, Fuqu and others), or the Korean nuruk. In most cases, the role of these starters is to produce enzymatic pools (mainly amylases, proteases, lipases) to hydrolyze substrate macromolecules (like starch, proteins, fatty acids) (e.g. rice, in the case of sake). The traditional Japanese koji is prepared using soybean grains as substrate, or other cereals like wheat and rice. The process is generally uncontrolled, the environment must be warm and humid, and the most frequent mold find in koji is A. oryzae, although other Aspergillus sp. (notably Aspergillus sojae), Rhizopus sp., Mucor sp., Monascus sp. and Penicillium sp. are also found in several cases (Zhu & Tramper, 2013). The Korean nuruk can be prepared with a diversity of cereals, but traditionally it is wheat based. The micro flora is also diverse, but the common involved genera are: Aspergillus, Mucarales and Rhizomucor. It is used to prepare an alcoholic beverage, similar to sake, called makgeolli (Bal, Yun, Yeo, Kim, & Kim, 2016). The Chinese daqu is divided basically in four types (light flavor, strong

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

Recent developments and innovations in solid state fermentation flavor, sauce flavor and miscellaneous flavor). Most of daqus are prepared with barley and pea, and are used as ingredients for several types of vinegar and liquors, among other products. Depending on the stage of the daqu preparation, several groups of microorganisms can be found, including mesophilic bacteria and fungi, yeasts and molds, lactic acid bacteria, and even thermophilic Bacillus and fungi (mainly Lichtheimia corymbifera) (Zheng et al., 2014). Recently, much attention has been paid to these starters. The following themes can be cited: cooking and mechanical conditions of fermentation (Jao, Ko, & Hsu, 2011); changes in environmental content affecting the flavor of products (Chen, Wu, & Xu, 2014); aroma development (IizukaFurukawa, Isogai, Kusaka, Fujii, & Wakai, 2016); detection and quantification and/or analysis of volatiles in koji derived products (Inoue et al., 2016; Moy, Lu, & Chou, 2012); different combinations of substrates for microorganism growth and/or biomolecules production (Chancharoonpong, Hsieh, & Sheu, 2012); production and/or role of enzymes (Kawauchi & Iwashita, 2014; Watanabe et al., 2011); metabolism of ferulic compounds --- which confer off flavors in final products (Hashizume, Ito, Ishizuka, & Takeda, 2013; Ito, Suzuki, Nakayama, Ito, & Hashizume, 2014; Suzuki, Ito, Hiroshima, Tokiwano, & Hashizume, 2016); anti-cholesterol effect of koji derived products (Lim et al., 2015); antioxidant effect of koji derived products (Feng et al., 2014; Giri, Osako, Okamoto, Okazaki, & Ohshima, 2011; Huang, Lai, & Chou, 2011; Ohata, Uchida, Zhou, & Arihara, 2016; Okutsu et al., 2012, 2015); supplementation of koji derived products (Marui et al., 2013); analysis of secreted proteins and/or peptides in koji related products (Maeda, Okuda, Hashizume, Joyo, & Mikami, 2011; Zhang, Guan, Cao, Xie, & Lu, 2015); importance of symbiosis (Furukawa, Watanabe, Toyama, & Morinaga, 2013) and finally, special attention has been given for the identification of microbial community in these complex environments (Bal et al., 2016; Felder, Burns, & Chang, 2012; Kim et al., 2015; Lv et al., 2013, 2015; Takashita et al., 2013; Tanaka, Watanabe, & Mogi, 2012; Wei et al., 2013; Yamada et al., 2011; Yan, Qian, Ji, Chen, & Han, 2013). Among the western classical products, the manufacturing of cheese can be cited as an example of classical employment of SSF. For some kinds of cheese, like the blue cheeses (e.g. Roquefort) and the soft cheeses (e.g. camembert) the ripening process is an important step, and can be either a spontaneous process, with naturally occurring strains or with selected starter cultures (SSC). In the last decades, food industry has focused attention on SSC for cheeses, in order to preserve safety and quality of the final product, besides its standardization (Bassi, Puglisi, & Cocconcelli, 2015). Regarding cheese and cheese-making process, papers in the last few years have reported the identification of the present microbiota (Gkatzionis, Yunita, Linforth, Dickinson, & Dodd, 2014), the gene transfer among fungi (Ropars et al., 2015) the activity of released enzymes (Ozturkoglu-Budak, Wiebenga, Bron, & de Vries, 2016), organoleptic and sensory characteristics (Galli, Martin, da Silva, Porto, & Spoto, 2016), the effect of milk treatment in the ripening process (Voigt, Patterson, Linton, & Kelly, 2011), dynamic mathematical modeling (Sicard, Baudrit, Leclerc-Perlat, Wuillemin, & Perrot, 2011), development of new tools for quality control (Sicard et al., 2012) and

7

functional (neuroprotective) effects of produced metabolites (Ano, Hoshi, Kutsukake, & Nakayama, 2016).

Others Many other applications can be found for SSF. Some of the most important ones are listed in Table 2, namely: organic acids production (Ali, Anwar, Irshad, Mukhtar, & Warraich, 2016; Das, Brar, & Verma, 2015; Das, Brar, & Verma, 2016; Dhillon, Kaur, Sarma, & Brar, 2013; Mai, Lee, & Choi, 2016; Raza et al., 2011); pigments production (Certík, Adamechová, & Guothová, 2013; Dursun & Dalgıc ¸, 2016; Eryılmaz, Dursun, & Dalgıc ¸, 2016; Haque, Kachrimanidou, Koutinas, & Lin, 2016; Srianta, Zubaidah, Estiasih, Yamada, & Harijono, 2016; Velmurugan et al., 2011); aroma production (Madrera, Bedrinana, & Valles, 2015); production/recovery of materials with potential use as biosorbents (Dhillon et al., 2016); production of phenolic compounds (Salar, Purewal, & Bhatti, 2016). Moreover, traditional processes, which are still being studied and improved by researchers: biobleaching (Cheng et al., 2012), ensiling (Ambye-Jensen et al., 2013; Franco, Buffiere, & Bayard, 2016; Kholif, Elghandour, Rodríguez, Olafadehan, & Salem, 2016) and composting (Fdez-Güelfo, Álvarez-Gallego, Sales, & García, 2012; Grujic, Dojnov, Potocnik, Duduk, & Vujci, 2015; Zhang, Zhang, Wang, Chen, & Wang, 2016). All these researches that are related to SSF bring light and new perspectives for important areas, such as food industry, tannery industry, animal feed industry, renewable energy industry and solid waste disposal/management.

Bioreactor design for SSF Since Raimbault started to work with packed bed columns, the so called Raimbault columns, some SSF bioreactors models appeared, which are classified as follows. Actually, SSF bioreactors can be classified based on the mixing system that is employed: static bioreactors (fixed bed, perforated trays) or stirred bioreactor (horizontal drum or stirred drum). Other classifications can be also found according to the type of aeration (with or without forced aeration) (Durand, 2003; Bhattacharyya, Banerjee, & Ghosh, 2008; Spier, Vandenberghe, Medeiros, & Soccol, 2011) or employed mixing system (Singhania et al., 2009). These are the tray, packed-bed, horizontal drum and fluidized bed bioreactors having their own advantages and disadvantages, which promoted the necessity to develop novel bioreactors with better design. Durand (2003) has given relevant information on various designs of bioreactor for SSF. The design of bioreactors must take into account some peculiarities of the materials that are used as growth media, and their characteristics such as composition, size, strength, porosity and water holding capacity. SSF occurs in the absence of free water and filamentous fungi are the microorganisms that are naturally adapted to this fermentation technique. In this case, some details must be considered in bioreactor design such as fungus morphology, with respect to the presence of septate hyphae or not, which influences the choice of agitation (without stirring, stirring occasionally or continuously). Another point to consider is the aeration by diffusion or forced aeration. All these details certainly raise bioreactors complexity.

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Microorganism

Substrate/support

Productivity

Bioreactor

Reference

Pigments Pigments

Monascus purpureus

Rice, corn, whole sorghum grain, dehulled sorghum grain and sorghum bran Wheat wastes

Highest peak is EMS (×103 ) 18895 for rubropunctamine, with rice as substrate 109.23 ␮g/g, 12 days (288 h)

A jar with 20 g of substrate

Srianta et al. (2016)

Static flasks

Dursun and Dalgıc ¸ (2016)

Olive pomace

220.24 ␮g/g, 12 days (288 h)

Static flasks

Eryılmaz et al. (2016)

Corn cob powder

25.42 OD units/g, 168 h

Static flasks

Velmurugan et al. (2011)

Wheat bran, rye bran, oat flakes, barley groats and spent malt grain

8.5 ␮g/g of ␤-carothene and 12.1 mg of ␥-linolenic acid, 180 h

Certík et al. (2013)

Bakery waste

24 AU (absorbance units)/g; 8 U and 117 U respectively for pigments, glucoamylase and protease, 168 h

Autoclavable microporous polypropylene bags (160 mm × 270 mm) Static flasks

Apple pomace

294.2 g/kg of dried apple pomace, 120 h 13.32 mg/g of substrate, 48 h

12 L rotating drum type bioreactor Static flasks

Dhillon et al. (2013)

41.45 g/kg of dry weight substrate, 21 days (504 h)

Static flasks

Das et al. (2016)

Pigment (astaxanthin)

Pigment (astaxanthin)

Pigments (red) ␤-Carothene and ␥-linolenic acid

Pigment, glucoamylase and protease Organic acids Citric acid Citric acid

Aspergillus niger NRRL 567 Consortium of Aspergillus ornatus and Alternaria alternata Rhizopus oryzae 1526

Apple pomace and peanut shell Pulp and paper solid waste

Haque et al. (2016)

Ali et al. (2016)

C.R. Soccol et al.

Fumaric acid

Yamadazyma guilliermondii, Yarrowia lipolytica, Xanthophylomyces dendrorhous, Sporidiobolus salmonicolor Xantophylomyces dendrorhous, Sporidiobolus salmonicolor Monascus purpureus KACC 42430 Mucor petrinsularis, Mucor dimorphosporus, Mucor circinelloides, Mucor hiemalis Monascus purpureus

ARTICLE IN PRESS

Product

+Model

Production of pigments, organic acids and other compounds by SSF in the last 5 years.

BIORI-2; No. of Pages 20

8

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Table 2

Substrate/support

Productivity

Bioreactor

Reference

Fumaric acid

Rhizopus oryzae 1526

Apple pomace

Lactobacillus amylovorus

Corn grits

Poli-gammaglutamic acid

Bacillus amyloliquefaciens

43.7 mg/g of substrates, 48 h

Oxalic acid

Aspergillus niger van Tieghem KACC 44333

Dairy manure compost, soybean cake, corn flour, residues from production of monosodium glutamate, wheat bran and rapeseed cake Corn cob powder

Plastic trays (35 cm × 22 cm × 11 cm) Lab scale stirred tank reactor Static flasks

Das et al. (2015)

Lactic acid

52.0 g/kg of dry weight substrate, 21 days (504 h) YP/S of 0.91 g/g

120 g/kg of dry weight substrate, 168 h

Static flasks

Mai et al. (2016)

Aspergillus awamori

Pearl millet

Static flasks

Salar et al. (2016)

Saccharomyces cerevisiae, Hanseniaspora valbyensis and Hanseniaspora uvarum Aspergillus niger

Apple pomace

176.82 mg GAE/g of dry substrate Esters, lactones, acids, terpenoids, aldehydes, ketones and alcohols --- a total of 144 compounds were produced

30 L capacity high density polyethylene (HDPE) tanks equipped with an air-lock

Madrera et al. (2015)

12-L rotating drum type bioreactor

Dhillon et al. (2016)

Others Phenolic compounds Volatile compounds

Biosorbents

Apple pomace

The different waste BMs, such as fungal biomass (living and dead), alkali insoluble material and acid and alkali insoluble material had their bioadsorbent potential (for metals) tested

Trontel et al. (2011) Yong et al. (2011)

YP/S , product yield from substrate (g g−1 ).

ARTICLE IN PRESS

Microorganism

+Model

Product

BIORI-2; No. of Pages 20

(Continued)

Recent developments and innovations in solid state fermentation

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

Table 2

9

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

10

Static bioreactors Different types of static bioreactors are used for SSF from laboratory to industrial scale. Erlenmeyer flasks, small perforated trays, fixed bed bioreactors or Raimbault columns, Petri dishes, jars, Roux bottles and roller bottles offer the advantage of simplicity and the possibility to work with small volumes. The main characteristic of these bioreactors is the absence of agitation (Durand, 2003). Erlenmeyer flasks are very simple and are used in laboratory scale for initial studies and processes’ conditions optimization. They are made of glass and have limited size. These flasks are closed with cotton plugs, which allow the aeration by diffusion. Some advantages are: easy of handle, low cost and allow multiple simultaneous tests. Different types of static bioreactors for SSF are presented below (Singhania et al., 2009; Spier et al., 2011).

Fixed bed bioreactors --- the Raimbault columns The Raimbault columns, packed bed or fixed bed bioreactors (Raimbault & Germon, 1976) are filled with the solid substrate or supports. The column bioreactors are closed systems with forced aeration. Columns are connected to air bubblers, and introduced into a water bath with controlled temperature. Aeration, made by saturated air that is pumped through the columns, is adjusted to the desired air flow and controlled with the help of a flowmeter attached to the column air outlet. This model of bioreactors allows the study of the influence of forced aeration on growth through the evaluation of respirometry (O2 consumed and CO2 produced) of the microorganism for the understanding of their metabolism. These bioreactors are the most employed in laboratory scale. A model of columns reactors made of glass coupled with a system that analyses the oxygen and carbon dioxide composition in the exhaust airflow from the column is shown in Fig. 1A. Limited bacterial contamination is observed due to the close system. Moreover, the same bioreactor can be used for both fermentation and extraction procedures of the final product (Singhania et al., 2009; Spier et al., 2011). The use of column reactors minimizes problems with temperature gradients, due to the convection caused by air entering the reactor. These bioreactors have been considered interesting due to process control, especially by removing heat (which does not happen efficiently in large-scale processes). Furthermore, the CO2 released during metabolic reactions can be eliminated, allowing its replacement by air, which is an advantage for some processes. Temperature control is done by placing the reactor in a bath or using jackets with circulating coolant fluid. However, the reduction in porosity of the bed, with the progress of fermentation, is a problem to overcome in this type of bioreactor. So the basic design feature of packed-bed bioreactors is the introduction of air through a sieve which supports the substrate. In this way, a bioreactor was developed at prepilot scale (Fig. 1C) for defining the control strategy and optimizing the air-inlet temperature, the airflow rate, the addition of water and agitation during a SSF process. Located in a clean room, the reactor can be pasteurized in situ by steam generated by the water-bath used for the air humidification. This reactor is very simple and can process a few

C.R. Soccol et al. kilograms of dry solid medium. An adaptation of packed bed bioreactors would be the insertion of mixing coupled with forced aeration, which could increase the homogeneity of the cell population. The geometry of the stirred bed reactor is similar to that used in fixed bed, but includes a mixing system. In this case, the great advantage of this system would be the possibility to work with higher scales (Singhania et al., 2009; Spier et al., 2011). Perforated trays bioreactors Tray bioreactors are simple systems in which the substrate is laid out on trays, made by wood or stainless steel, which are perforated to facilitate air convection Fig. 1B. The substrate is placed in the tray in thin layers (from 5 to 15 cm) that are arranged with a space between them to allow the aeration. Trays are arranged in a chamber or room with controlled temperature and humidity. This model is easy to scale-up, but requires large areas for operations, intensive labor and difficulties with contamination control (non sterile processes). Problems can also occur with oxygen transfer, which depends on tray characteristics and the height of the substrate layer. When the substrate is inoculated, the oxygen concentration is uniform. Then, the formation of the mycelium changes the porosity and thus the effective diffusivity. The release of CO2 and heat also limit the transport of O2 and the creation of higher O2 gradients that are inevitable, especially for higher substrate layers.

Agitated bioreactors Another concept of bioreactors for SSF, which was based on continuous or intermittent agitation of the solid medium, was also developed (Durand, 2003; Spier et al., 2011; Thomas, Larroche, & Pandey, 2013). The bioreactors can be a rotating drum or horizontal paddle mixer with or without a water-jacket. When working with continuously mixing, it is expected to increase the homogeneity of the solid medium and better oxygen transfer to the microorganism. Koji bioreactors An example of static non-sterile bioreactor is represented by the rotary type automatic Koji making equipment marketed by Fujiwara in Japan (Fig. 2A). The treated substrate is heaped up on a rotary disk. Depending on the diameter of this disk, different working volumes are available but always with a layer of maximum thickness 50 cm. This non-sterile reactor operates with a microcomputer which controls all the parameters (temperature of the air-inlet, air flow rate and agitation periods). The main drawback of this equipment is the need to prepare and inoculate the substrate in other equipment before filling the reactor. Nevertheless, this type of design is widely used in Asian countries (Durand, 2003; Singhania et al., 2009; Spier et al., 2011). Horizontal drum Horizontal drum bioreactors are built in drum-shape and contain baffles for agitation of the medium (Fig. 2B). The agitation in this type of reactor can be continuous or sporadic, and may lead to problems of shear and damage of the mycelium structure. The schematic system is showed in

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model

ARTICLE IN PRESS

BIORI-2; No. of Pages 20

Recent developments and innovations in solid state fermentation

A

11 5

4

B

8

9

8 6

7

2 14

7

10

3 15

4

9

5

11

1

12

1

6

14

3

C 1

1 2

2

3

4 6

5

5

TºC RH Air

Water LP Water 8

7 9

Figure 1 (A) Lab-scale fixed bed bioreactors apparatus for solid state fermentation: (1) air pump; (2) air distribution system; (3) humidifiers; (4) fermentation columns immersed in a water bath with controlled temperature; reactor; (5) filter; (6) flow sensor; (7) controllers display; (8) computer with data acquisition and control software; (9) cylindrical sensor base, where the following sensors are installed: CO2 and O2 , humidity and outlet temperature. (B) Perforated trays bioreactor. (C) Unmixed bioreactors with forced aeration. (1) Basket containing the solid medium, (2) valves for airflow adjustment, (3) air temperature probe, (4) relative humidity probe, (5) draincocks, (6) heating box, (7) humidifier, (8) coil for circulation of cold water, (9) resistive heater. Sources: modified from Durand (2003), Spier et al. (2011) and Singhania et al. (2009).

Fig. 2B. This bioreactor has been used for solid-state fermentation since the 1930s (Durand, 2003).

Mixing bioreactor A 50 L bed bioreactor was patented by Durand (2003). This reactor, which has a planetary mixing device (Fig. 2C) and is completely automatic for the different process steps: sterilization of the bioreactor, sterilization of the medium, process control during fermentation and data acquisition.

is no agitator within the substrate bed (Fig. 2D). The engineering principles of RDB have received interest for biofuels production using cellulosic materials (Durand, 2003; Spier et al., 2011). Rotating drum bioreactors with air circulation and continuously mixing are commonly used in pilot or lab scale process. According to Durand (2003) the largest reactor cited in the literature was a 200 L stainless steel rotating drum, which used 10 kg of steamed wheat bran as substrate for kinetic studies of Rhizopus.

Scale-up aspects Rotating drum Rotating drum bioreactors (RDB) consist of an horizontal cylinder, where the mixing is provided by the tumbling motion of the solid medium, which may be aided by baffles on the inner wall of the rotating drum (perforated or not). However, in all these reactors, the mixing is less efficient than with a paddle mixer. RDBs provide relatively gentle and uniform mixing by improving baffle design, since there

Although scale-up methods for SmF are well developed, these methods cannot be applied directly to SSF bioreactors: due to the differences in the physical structures of the systems (Pandey, 2003; Singhania et al., 2009; Soccol & Vandenberghe, 2003). The major problems to overcome are related to the engineering aspects, such as lack of standardized processes and limited reproducibility of the

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model

ARTICLE IN PRESS

BIORI-2; No. of Pages 20

12

C.R. Soccol et al.

A

B 1

7

12

11 10

3 4

8

10

11 12

5

8 8

222

9 5

9 1

6

C

2

Ar

7

4

3

M

6

D M IS

CO

F

AIR

5

9

4

LH BP HB

3 TP

2

AD JR

HC AT

CB

HM

SH 1 WG STEAM

8

7

6

Figure 2 (A) Koji making equipment: (1) Koji room, (2) rotating perforated table, (3) turning machine, (4, 11) screw and machine for unloading, (5) air conditioner, (6) fan, (7) air outlet, (8) dampers (9) air filter, (10) machine for filling, (12) control board. (B) Schema horizontal drum: (1) compressor, (2) Air filter, (3) humidifier, (4) horizontal drum, (5) stirrer, (6) motor, (7) speed controller, (8) air discharge, (9) silica gel columns, (10) element name (11) gas chromatograph (12) computer. (C) Sterile bioreactor developed by the National Institute of Agronomic Research in Dijon (F) Air filter, (HC) humidification chamber, (HB) heating battery, (BP) bypass, (CB) cooling battery, (HM) probe for air relative humidity measurement, (TP) probe for medium temperature measurement, (WG) weight gauges, (SH) sterile sample handling, (JR) water temperature regulation in the double jacket, (AD) planetary agitation device, (M) motor for agitation, (IS) sterile system for adding inoculum and solutions, (CO) water air condenser. (D) Rotating drum bioreactor. (1) Air-inlet, (2) rotating joint, (3) coupling, (4) air nozzles, (5) air line, (6) rollers, (7) rotating drum, (8) solid medium, (9) rim. Sources: Modified from Durand (2003), Singhania et al. (2009) and Spier et al. (2011).

experimental results. A large number of patents and publications are available on how to design, operate and scale-up SSF bioreactors. Difficulties to scale-up are related to the intense heat generation and heterogeneity of the system. The microbial growth under aerobic conditions results in considerable heat production that causes a fast increase of temperature. This effect is undesirable especially in some biotechnological processes of heat sensible products or enzymes that can be heat-denatured. The water lost by evaporation has to be in many cases replenished, and this can lead to undesirable local increase in water activity during static processing. Several bioreactor designs have been developed in an attempt to combat these problems, but only a few have been used at large-scale, and information available about their performance is increasing in the form of original research articles as well as reviews (Singhania et al., 2009; Spier et al., 2011; Thomas et al., 2013). From the above studies, it could be concluded that efforts have been made to modify the known design of SSF

bioreactors. New information has been generated on the impact of process parameters such as aeration to better define the heat and mass transfer effects. Thus, while the basic designs of the bioreactors have remained the same, a lot new information has been generated on their modification, or on other processing aspects.

Recent patents and innovations Patents can be used as a source of information about all sorts of technologies. When a technology is patented, specific knowledge about its novelty, inventiveness and industrial applications must be disclosed. Besides, it is possible to infer indirect information about it, such as its origin, history and state of development. Due to the requirements for a patent to be granted, it is possible to say that a patent document has the newest information compared to the state of the art. On top of that, it is presumable that a patented invention

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model

ARTICLE IN PRESS

BIORI-2; No. of Pages 20

Recent developments and innovations in solid state fermentation

40% 30% 20%

714

7%

7%

rs O th e

er at Fe d

us si a R

Pa t n ea op

n

en

d

tO

St a

io n

ffi ce

te

s

ea ni te U

ub lic 2011−2016

Eu r

1963−1970 1971−1980 1981−1990 1991−2000 2001−2010

ep

32

R

10

7%

Ko r

hi na C

0

109 3

7%

0%

400 200

11%

8%

10%

of

600

54%

Ja pa n

800

350 300 250 200 150 100 50 0 20 09

1000

60% 50%

20 11 20 13 20 15

1200

1303

20 01 20 03 20 05 20 07

Worldwide patent applications

1400

13

Figure 3 Evolution of patent applications related to SSF technologies, since 1963.

Figure 4 Distribution of SSF-related patent applications between the countries that contribute more to this technology development.

have a well-defined industrial application, and is nearing a commercially availability. When combined with complementary data, they provide a basis for a broad analysis of various dimensions of innovations, as the role of intellectual property, of economic performance, entrepreneurship and on search for links in science and technological development (Ferreira da Costa, Soccol, & Soccol, 2016; OECD, 2009; WTO, 1994). In this context, it is important to analyze any specific technology using this data. The first patented invention regarding SSF was filed in 1962 by Riker Laboratories, Inc., today subsidiary of 3M Company. This invention aimed to produce a pyrogen-free penicillinase and was used in injection therapy for combating allergic sensitivity to penicillin (Riker, 1962). According to Pandey (2003) this technology was not used in the western countries until the 1940s, due to the development and wide use of submerged fermentation. SSF only became subject of study from 1950 on, on a slow pace. It was after the end of the 1990s that the interest in this technology boomed. Almost 93% of the total worldwide patent applications regarding SSF (2178) were filed after 2001, as illustrated in Fig. 3. The trend from 2001 to 2016 is highlighted on the chart. It is evident the raise in the number of applications is continuous. There has been no considerable decrease in such filings, since 2001. No peak has been reached yet, and there is no sign of a change of pace, as the number of patent applications is still trending upwards. The apparent decrease in 2016, when compared to 2015, may be explained by the fact that the year is yet to end and the 18-month secrecy period of every patent application. The latter may also be responsible for an underestimation of 2015’s numbers, which would help to steep down the growth curve. Fig. 4 presents the distribution of SSF related patent applications, filed through the Patent Cooperation Treaty (PCT), a system used to ease international applications. Therefore, the presented data ignores resident applications and may underestimate the relevance of some countries that traditionally does not file patents overseas. China is the country with more patent applications in the world, with a large margin to Japan, South Korea, United States, European Union and Russia. This is probably due to the fact that this technology has only recently attracted interest from western scientists and industries, due to its

applicability in production of several products using industrial residues as substrate. Also, SSF has been used in China for food and beverage production for thousands of years, and continues to be relevant to date. Over 80% of fermented foods and beverages, such as soy sauce, vinegar, distilled spirits, sufu, lobster sauce and mushrooms, produced in China are made via SSF (Liu et al., 2004; Wei, 2001). Brazil, as one of the most important agricultural countries in the world, carries a strong potential for SSF due to its high availability of solid residues, commonly used as substrate in this kind of fermentation. It does not appear in the worldwide ranking, but it has been filing a considerable number of patents in its local patent office (173). It is important to mention a specific group in Curitiba that has contributed immensely to the development of SSFrelated technologies in Brazil: the Department of Bioprocess Engineering and Biotechnology in Universidade Federal do Parana has been one of the most prolific research group in that area, filing patents since the end of the 1990s, being strong in transforming agro-industrial residues in high-value products. Relevance of said group was already discussed by Soccol and Vandenberghe (2003). A patent, when filed, receives at least one International Patent Classification (IPC), which may refer to its function and/or its application. A patent may receive more than one IPC and, usually, this classification considers the additional information to the state of the art, including the invention’s novelty, inventiveness and industrial application (WIPO, 2016). Through the analysis of this data the patent applications were segmented according to their received IPC, as presented in Fig. 5. SSF-related patents are classified in many different classes, but most of them regard food and beverage technologies. Over 30% of the patents were classified as novel to the food or beverage industry. Those included fermented alcoholic and non-alcoholic beverages, such as milk, wine, beer, vinegar, and the modification of foods, comprising most oriental fermented foods. Several patents regards the development and production of animal feed. Most of them use fermented residues to increase the quality of such products. It is important to notice the number of patents regarding development and/or modifications made to bioreactors. This trend is something already anticipated and discussed by Singhania et al. (2009) to improve SSF efficiency and help its

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model

ARTICLE IN PRESS

BIORI-2; No. of Pages 20

14

C.R. Soccol et al. Food or beverage Animal feed

Bioreactor engineering Fuels (Ethanol, buthanol) Fertilizers Waste treatment Sugars (saccharification) Production of enzymes Medicinal preparations Others 0%

5%

10%

15%

20%

25%

30%

35%

40%

Figure 5 Patent applications classified according to their function or application.

scale-up process, which is pointed as one of the most important drawbacks of this technology to make it commercially feasible. Other interesting areas receiving attention are fuels production (mainly ethanol and butanol), waste treatment, production of enzymes and saccharification. A lot of inventions that received this IPC aimed to produce biofuels from lignocellulosic residues, a technology that comprises several diverse processes, such as biomass treatment (waste treatment) to produce fermentable sugars (saccharification), enzymatic hydrolysis of cellulose (production of enzymes) and fermentation of sugars (polysaccharides, such as cellulose, or monosaccharides, such as glucose and xylose). Production of enzymes is a well-known application of SSF. Production of phytase, amylase, inulinase, cellulase, protease, alpha-galactosidase, lipase, tannase, laccase, chitinase, l-glutaminase, lipase was widely studied and reviewed (Singhania et al., 2009). Production of fertilizers and pharmaceuticals, mainly antibiotics, also appear constantly in recent patent and inventions. In order to assess the technologies that have been receiving most attention in the past 10 years, the most cited patents regarding SSF were reviewed. Brown et al. (2005) describes a process for production of recombinant enzymes, including cellulase, endoglucanase, cellobiohydrolase and beta-glucosidase with cellulolytic activity, in order to treat cellulosic material, such as agricultural of forestry residue, solid waste, waste paper, or pulp and paper mill residue, or corn stover. The invention also comprises a saccharification and fermentation process, whereas the latter is made via SSF of the treated biomass, with the enzymes produced in the previous step. Product of this fermentation may be several, including alcohol, organic acid, ketone, amino acid, or gas. The main novelty of this patent resides on the amino acid sequences of the produced enzymes, alongside with the nucleotide sequences to translate them in recombinant microorganisms. Several microorganisms comprising these sequences are also claimed by the patent. They describe the production process of the enzymes, adding several applications and examples of use. Following the same pattern, Lombard (2001), Fukuyama et al. (2006), Vlasenko, Cherry, and Xu (2005), Berka and Cherry (2005), Boerge and Lena (2007), Krogh and Harris (2007) and Huang et al. (2010) describe different processes to perform a simultaneous saccharification and SSF process to produce ethanol from lignocellulosic

materials. The main novelty of those inventions vary widely, from the hydrolysis of hemicellulose, removal of lignin and, mainly, the enzymes produced. Suryanarayan, Mazumdar, and Mazumdar (2000) presents a modular bioreactor for cultivating microorganisms in solid medium. The base modulus contains communicating channels that are used to control several parameters of the fermentation, such as temperature and aeration. Other moduli may be stacked on top of each other, independently, and may be individually controlled. The bioreactor is closed to avoid contamination and comprises an agitation system. As the bioreactor is modular, it is totally adjustable and easy to disassemble. In the patent several examples of application are described. The modular aspect of this bioreactor is considered as the main novelty of this invention. Other modular bioreactors are presented in patents from Gorwalla and Kulkarni (2010) and Lueth and Wismar (2005). An automatic chain-belt-type bioreactor for SSF is described by Lang and Zhang (2010). It is a sequential reactor, with the inoculating tank being connected with the fermentation reactor, through a spiral transmitter, which is noted as the main novelty of this apparatus. The transmission and withdrawal of materials are done automatically, so that the input to the second fermenter receives the output from the first one (inoculating tank). Patent Hoelker, Janssen, and Lenz (2004) also presents a chain-belt-type fermenter for SSF. Most recent patent applications regarding bioreactor engineering have been focusing on improved controlling systems, stirring apparatus and adaptations for continuous cultures, including connections with downstream processes (Alitalo, Aura, & Niskanen, 2016; Hou et al., 2016; Kim, Liu, & Zhang, 2016; Lai, Xue, & Yang, 2016). A method for producing organic fertilizer through anaerobic fermentation of solid waste, via SSF, is claimed by Du, Wang, Wang, Xu, and Zhao (2009). The invention comprises the preparation of different solid wastes, comprising steps for mixing it and regulating water content. Acidic and anaerobic fermentations are described in this patent. The main goal of the invention is to produce humic acid granule fertilizer. As stated above, several patents regarding SSF are useful for food and beverage production or improvement. The products are very diverse, including vinegar (Cao, 2014; Li, 2009; Wang, Gao, & Yao, 2006), soy sauce and Koji (Lim, Ng, Heyland, & Dac, 1999; Liu, Wu, Yang, & Zhou, 2009; Yu, 2011), wines and spirits (Ao et al., 2009; Huang, Ji, Li, & Wang, 2009), food additives (Chen & Zhuang, 2008; Gao, Lu, & Yan, 2013; Sobol & Sobol, 2003), cereals (Jiang, Wang, Jiang, & Zhu, 2011; Sun, 2007). More recently, focus has been on technologies for production of foods and beverages with medicinal properties, such as antioxidant activity, lowering blood fat, helping digestion, promoting better blood circulation, among others (Cheng, Cheng, et al., 2016, Cheng, Fu, et al., 2016; Feng, 2016; Hu et al., 2016; Liu, Song, et al., 2016).

Conclusions Solid-state fermentation (SSF) is an alternative fermentation technique whose characteristics allow the re-use

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

Recent developments and innovations in solid state fermentation of agro-industrial and/or sub-products as substrate support for biotechnological production of low to high value biomolecules. It is very well stablished for certain traditional processes such as fermented food in the oriental countries. As it presents various advantages for certain processes, it still attracts much attention by many researchers worldwide. It is not surprising that a technology so elegantly simple continues to raise attention of scientists and industries around the globe, as shown by the patent data herein. As its potentials and applications are extremely diverse, there are important drawbacks yet to be solved, and there is no reason for a decrease in patent applications in the foreseeable future. The potentialities and advantages of SSF must be evaluated for each process. However, it is clear that some limitations for the scale-up are still observed. In this case, the choice of the microorganism, substrate/support and bioreactor are predominant and, of course, the economic viability depends on a careful comparison of SSF and submerged fermentation processes.

Acknowledgments Authors want to thank to CAPES and CNPq for the financial support.

References Adhyaru, D. N., Bhatt, N. S., Modi, H. A., & Divecha, J. (2016). Insight on xylanase from Aspergillus tubingensis FDHN1: Production, high yielding recovery optimization through statistical approach and application. Biocatalysis and Agricultural Biotechnology, 6, 51---57. Afrisham, S., Badoei-Dalfard, A., Namaki-Shoushtari, A., & Karami, Z. (2016). Characterization of a thermostable, CaCl2 -activated and raw-starch hydrolyzing alpha-amylase from Bacillus licheniformis AT70: Production under solid state fermentation by utilizing agricultural wastes. Journal of Molecular Catalysis B: Enzymatic, 132, 98---106. Ali, S. R., Anwar, Z., Irshad, M., Mukhtar, S., & Warraich, N. T. (2016). Bio-synthesis of citric acid from single and co-culturebased fermentation technology using agro-wastes. Journal of Radiation Research and Applied Sciences, 9, 57---62. Alitalo, A., Aura, E., & Niskanen, M. (2016). Bioreactor and fermentation process for producing hydrogen. PCT Patent Application WO2016097478, 23 Jun 2016. Ambye-Jensen, M., Johansen, K. S., Didion, T., Kadar, Z., Schmidt, J. E., & Meyer, A. S. (2013). Ensiling as biological pretreatment of grass (Festulolium Hykor): The effect of composition, dry matter, and inocula on cellulose convertibility. Biomass and Bioenergy, 58, 303---312. Ang, S. K., Shaza, E. M., Adibah, Y., Suraini, A. A., & Madihah, M. S. (2013). Production of cellulases and xylanase by Aspergillus fumigatus SK1 using untreated oil palm trunk through solid state fermentation. Process Biochemistry, 48, 1293---1302. Ano, Y., Hoshi, A., Kutsukake, T., & Nakayama, H. (2016). Neuroprotective effects of dehydroergosterol identified in Camembert cheese via suppression of microglial inflammation. Alzheimer’s & Dementia, 12(7), 863. Ao, Z., Shen, C., Shui, L., Wang, Q., Xu, D., Yi, B., et al. (2009). Method for producing aroma type customized wine. Chinese Patent Application CN101457189, 17 Jun 2009. Bal, J., Yun, S.-H., Yeo, S.-H., Kim, J.-M., & Kim, D.-H. (2016). Metagenomic analysis of fungal diversity in Korean traditional

15

wheat-based fermentation starter nuruk. Food Microbiology, 60, 73---83. Bassi, D., Puglisi, E., & Cocconcelli, S. (2015). Comparing natural and selected starter cultures in meat and cheese fermentations. Current Opinion in Food Science, 2, 118---122. Bansal, N., Tewari, R., Soni, R., & Soni, S. K. (2012). Production of cellulases from Aspergillus niger NS-2 in solid state fermentation on agricultural and kitchen waste residues. Waste Management, 32, 1341---1346. Berka, R., & Cherry, J. (2005). Methods for converting plant cell wall polysaccharides. US Patent Application US2005233423, 20 Oct. 2005. Bhattacharyya, B. C., Banerjee, S., & Ghosh, T. K. (2008). Bioreactors: functions in fermentation processes. In A. Pandey, C. Larroche, C. R. Soccol, & C. G. Dussap (Eds.), Advances in Fermentation Technology (pp. 172---201). New Delhi: Asiatech Publishers. Bhattacharya, S. S., Garlapati, V. K., & Banerjee, R. (2011). Optimization of laccase production using response surface methodology coupled with differential evolution. New Biotechnology, 28, 31---39. Biz, A., Finkler, A. T. J., Pitol, L. O., Medina, B. S., Krieger, N., & Mitchell, D. A. (2016). Production of pectinases by solid-state fermentation of a mixture of citrus waste and sugarcane bagasse in a pilot-scale packed-bed bioreactor. Biochemical Engineering Journal, 111, 54---62. Boerge, H. C., & Lena, H. C. (2007). Method and apparatus for conversion of cellulosic material to ethanol. PCT Patent Application WO2007009463, 25 Jan 2007. Brown, K., Harris, P., Zaretsky, E., Rey, E., Vlasenko, E., Mcfarland, K., et al. (2005). Polypeptides having cellulolytic enhancing activity and polynucleotides encoding same. PCT Patent Application WO2005074647, 18 Aug. 2005. Cabana, H., Jones, J. P., & Agathos, S. N. (2007). Preparation and characterization of cross-linked laccase aggregates and their application to the elimination of endocrine disrupting chemicals. Journal of Biotechnology, 132, 23---31. Cao, S. (2014). Preparation method of dried mushroom-sticky rice vinegar. Chinese Patent Application CN103695284, 02 Apr 2014. Castro, R. J. S., Ohara, A., Nishide, T. G., Bagagli, M. P., Dias, F. F. G., & Sato, H. H. (2015). A versatile system based on substrate formulation using agroindustrial wastes for protease production by Aspergillus niger under solid state fermentation. Biocatalysis and Agricultural Biotechnology, 4, 678---684. Cerda, A., El-Bakry, M., Gea, T., & Sánchez, A. (2016). Long term enhanced solid-state fermentation: Inoculation strategies for amylase production from soy and bread wastes by Thermomyces sp. in a sequential batch operation. Journal of Environmental Chemical Engineering, 4, 2394---2401. Certík, M., Adamechová, Z., & Guothová, L. (2013). Simultaneous enrichment of cereals with polyunsaturated fatty acids and pigments by fungal solid state fermentations. Journal of Biotechnology, 168, 130---134. Chancharoonpong, C., Hsieh, P. C., & Sheu, S. C. (2012). Effect of different combinations of soybean and wheat bran on enzyme production from Aspergillus oryzae S. APCBEE Procedia, 2, 68---72. Chanwicha, N., Katekaew, S., Aimi, T., & Boonlue, S. (2015). Purification and characterization of alkaline xylanase from Thermoascus aurantiacus var. levisporus KKU-PN-I2-1 cultivated by solid-state fermentation. Mycoscience, 56, 309---318. Chen, B., Wu, Q., & Xu, Y. (2014). Filamentous fungal diversity and community structure associated with the solid state fermentation of Chinese Maotai-flavor liquor. International Journal of Food Microbiology, 179, 80---84. Chen, S., & Zhuang, J. (2008). Cereal solid-state fermentation Chinese caterpillar fungus and ganoderma lucidum product,

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

16 and preparing method thereof. Chinese Patent Application CN101171968, 07 May 2008. Cheng, S. S., Chao, Y. C., Wong, S. C., Chen, C. C., Yang, K. H., & Yang, Y. F. (2012). Study on hydrogen production potential utilizing leachate from aerobic bio-leaching bed fed with napiergrass and kitchen waste. Energy Procedia, 29, 72---81. Cheng, J., Cheng, S., He, L., Yang, H., Wei, H., Hu, Z., et al. (2016a). Composition obtained by fermenting tetrastigma hemsleyanum diels et gilg. through edible and medicinal fungi and preparation method of composition. Chinese Patent Application CN105559068, 11 May 2016. Cheng, J., Fu, L., He, L., Li, H., Wei, H., Hu, Z., et al. (2016b). Inonotus obliquus fermentation culture composition and preparation method thereof. Chinese Patent Application CN105535035, 04 May 2016. Das, R. K., Brar, S. K., & Verma, M. (2015). A fermentative approach towards optimizing directed biosynthesis of fumaric acid by Rhizopus oryzae 1526 utilizing apple industry waste biomass. Fungal Biology, 119, 1279---1290. Das, R. K., Brar, S. K., & Verma, M. (2016). Potential use of pulp and paper solid waste for the bio-production of fumaric acid through submerged and solid state fermentation. Journal of Cleaner Production, 112, 4435---4444. Dhillon, G. S., Brar, S. K., Kaur, S., Metahni, S., & M’hamdi, N. (2012). Lactoserum as a moistening medium and crude inducer for fungal cellulase and hemicellulase induction through solidstate fermentation of apple pomace. Biomass and Bioenergy, 41, 165---174. Dhillon, G. S., Kaur, S., & Brar, S. K. (2012). In-vitro decolorization of recalcitrant dyes through an ecofriendly approach using laccase from Trametes versicolor grown on brewer’s spent grain. International Biodeterioration & Biodegradation, 72, 67---75. Dhillon, G. S., Kaur, S., Brar, S. K., & Verma, M. (2012). Potential of apple pomace as a solid substrate for fungal cellulase and hemicellulase bioproduction through solid-state fermentation. Industrial Crops and Products, 38, 6---13. Dhillon, G. S., Kaur, S., Sarma, S. J., & Brar, S. K. (2013). Integrated process or fungal citric acid fermentation using apple processing wastes and sequential extraction of chitosan from waste stream. Industrial Crops and Products, 50, 346---351. Dhillon, G. S., Rosine, G. M. L., Kaur, S., Hegde, K., Brar, S.K., Drogui, P., et al. Novel biomaterials from citric acid fermentation as biosorbents for removal of metals from waste chromated copper arsenate wood leachates. International Biodeterioration & Biodegradation (in press, Corrected Proof, Available online 20 September 2016). Du, W., Wang, J., Wang, Y., Xu, J., & Zhao, Y. (2009). Combined anaerobic fermentation process for organic solid wastes. Chinese Patent Application CN101337838, 07 Jan 2009. Durand, A. (2003). Bioreactor designs for solid state fermentation. Biochemical Engineering Journal, 363, 1---13. Dursun, D., & Dalgıc ¸, A. C. (2016). Optimization of astaxanthin pigment bioprocessing by four different yeast species using wheat wastes. Biocatalysis and Agricultural Biotechnology, 7, 1---6. El-Batal, A. I., ElKenawy, N. M., Yassin, A. S., & Amin, M. A. (2015). Laccase production by Pleurotus ostreatus and its application in synthesis of gold nanoparticles. Biotechnology Reports, 5, 31---39. Eryılmaz, E. B., Dursun, D., & Dalgıc ¸, A. C. (2016). Multiple optimization and statistical evaluation of astaxanthin production utilizing olive pomace. Biocatalysis and Agricultural Biotechnology, 7, 224---227. Farinas, C. S. (2015). Developments in solid-state fermentation for the production of biomass degrading enzymes for the bioenergy sector. Renewable and Sustainable Energy Reviews, 52, 179---188. Fdez-Güelfo, L. A., Álvarez-Gallego, C., Sales, D., & García, L. I. R. (2012). Dry-thermophilic anaerobic digestion of organic fraction

C.R. Soccol et al. of municipal solid waste: Methane production modeling. Waste Management, 32, 382---388. Felder, D., Burns, D., & Chang, D. (2012). Defining microbial terroir: The use of native fungi for the study of traditional fermentative processes. International Journal of Gastronomy and Food Science, 1, 64---69. Feng, Y., Chen, Z., Liu, N., Zhao, H., Cui, C., & Zhao, M. (2014). Changes in fatty acid composition and lipid profile during koji fermentation and their relationships with soy sauce flavor. Food Chemistry, 158, 438---444. Feng, Y. (2016). Brewing method of fragrant and sweet osmanthusflavored wine. Chinese Patent Application CN105462768, 06 Apr 2016. Fernández-Fernández, M., Sanromán, M. Á., & Moldes, D. (2013). Recent developments and applications of immobilized laccase. Biotechnology Advances, 31, 1808---1825. Ferrarezi, A. L., Ohe, T. H. K., Borges, J. P., Brito, R. R., Siqueira, M. R., Vendramini, P. H., et al. (2014). Production and characterization of lipases and immobilization of whole cell of the thermophilic Thermomucor indicae seudaticae N31 for transesterification reaction. Journal of Molecular Catalysis B: Enzymatic, 107, 106---113. Ferreira da Costa, E. S., Soccol, F. T., & Soccol, C. R. (2016). Patents on biofuels. In C. R. Soccol, S. K. Brar, C. Faulds, & L. P. Ramos (Eds.), Green fuels technology: Biofuels (pp. 501---523). Switzerland: Springer International Publishing. Fonseca, M. I., Fari˜ na, J. I., Castrillo, M. L., Rodríguez, M. D., Nu˜ nez, C. E., Villalba, L. L., et al. (2014). Biopulping of wood chips with Phlebia brevispora BAFC 633 reduces lignin content and improves pulp quality. International Biodeterioration and Biodegradation, 90, 29---35. Font, X., Caminal, G., Gabarrell, X., Romero, S., & Vicent, M. T. (2003). Black liquor detoxification by laccase of Trametes versicolor pellets. Journal of Chemical Technology and Biotechnology, 78(5), 548---554. Franco, R. T., Buffiere, P., & Bayard, R. (2016). Ensiling for biogas production: Critical parameters. A review. Biomass and Bioenergy, 94, 94---104. Freitas, A. C., Baleeiro, F. C. F., Fonseca, R. F., Bertucci Neto, V., Pinto, G. A. S., & Farinas, C. S. (2015). Bioprocess development to add value to canola cake used as substrate for proteolytic enzyme production. Food and Bioproducts Processing, 95, 173---182. Fukuyama, S., Matsui, T., Soong, C., Allain, E., Vikso-Nielsen, A., Udagawa, H., et al. (2006). Enzymes for starch processing. PCT Patent Application WO2006069290, 29 Jun 2006. Furukawa, S., Watanabe, T., Toyama, H., & Morinaga, Y. (2013). Significance of microbial symbiotic coexistence in traditional fermentation. Journal of Bioscience and Bioengineering, 116, 533---539. Galhaup, C., Goller, S., Peterbauer, C. K., Strauss, J., & Haltrich, D. (2002). Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology, 148, 2159---2169. Galli, B. D., Martin, J. G. P., da Silva, P. P. M., Porto, E., & Spoto, M. H. F. (2016). Sensory quality of Camembert-type cheese: Relationship between starter cultures and ripening molds. International Journal of Food Microbiology, 234, 71---75. Gao, X., Lu, J., & Yan, S. (2013). Aspergillus oryzae and application method thereof in preparing sauce fragrant flavor material. Chinese Patent Application CN102787079, 21 Nov 2012. Garai, D., & Kumar, V. (2013). A Box---Behnken design approach for the production of xylanase by Aspergillus candidus under solid state fermentation and its application in saccharification of agro residues and Parthenium hysterophorus L. Industrial Crops and Products, 44, 352---363. Giri, A., Osako, K., Okamoto, A., Okazaki, E., & Ohshima, T. (2011). Antioxidative properties of aqueous and aroma extracts of squid

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

Recent developments and innovations in solid state fermentation miso prepared with Aspergillus oryzae-inoculated koji. Food Research International, 44, 317---325. Gkatzionis, K., Yunita, D., Linforth, R. S. T., Dickinson, M., & Dodd, C. E. R. (2014). Diversity and activities of yeasts from different parts of a Stilton cheese. International Journal of Food Microbiology, 177, 109---116. Godoy, M. G., Gutarra, M. L. E., Castro, A. M., Machado, O. L. T., & Freire, D. M. G. (2011). Adding value to a toxic residue from the biodiesel industry: Production of two distinct pool of lipases from Penicillium simplicissimum in castor bean waste. Journal of Industrial Microbiology and Biotechnology, 38, 945---953. Gorwalla, E. P., & Kulkarni, S. N. (2010). Stacked basket bioreactor for solid state fermentation. PCT Patent Application WO2010032260, 25 Mar 2010. Gowdhaman, D., Manaswini, V. S., Jayanthi, V., Dhanasri, M., Jeyalakshmi, G., Gunasekar, V., et al. (2014). Xylanase production from Bacillus aerophilus KGJ2 and its application in xylooligosaccharides preparation. International Journal of Biological Macromolecules, 64, 90---98. Grujic, M., Dojnov, B., Potocnik, I., Duduk, B., & Vujci, Z. (2015). Spent mushroom compost as substrate for the production of industrially important hydrolytic enzymes by fungi Trichoderma spp. and Aspergillus niger in solid state fermentation. International Biodeterioration & Biodegradation, 104, 290---298. Hailei, W., Chaozhi, T., Guangli, Y., & Ping, L. (2013). A novel membrane-surface liquid co-culture to improve the production of laccase from Ganoderma lucidum. Biochemical Engineering Journal, 80, 27---36. Haque, M. A., Kachrimanidou, V., Koutinas, A., & Lin, C. S. K. (2016). Valorization of bakery waste for biocolorant and enzyme production by Monascus purpureus. Journal of Biotechnology, 231, 55---64. Hashizume, K., Ito, T., Ishizuka, T., & Takeda, N. (2013). Formation of ethyl ferulate by rice koji enzyme in sake and mirin mash conditions. Journal of Bioscience and Bioengineering, 116(2), 209---213. Hoelker, U., Janssen, M., & Lenz, J. (2004). Directed selective solidphase culturing of stable microbial mixed populations for the continuous preparation of defined enzyme and metabolite mixtures. PCT Patent Application WO2004113490, 29 Dec 2004. Hou, Z., Ma, Y., Ren, L., Tong, J., Tian, A., Hou, M., et al. (2016). Biomass continuous fermentation system. Chinese Patent Application CN105602841, 25 May 2016. Hu, Y., Li, D., Li, W., Wang, C., Shi, Y., Xu, N., et al. (2016). Garlic juice and mulberry vinegar. Chinese Patent Application CN105567544, 11 May 2016. Huang, J., Ji, L., Li, P., & Wang, S. (2009). Method for preparing spirit flavoring wine or spirit flavour liquid mainly with fragrance. Chinese Patent Application CN101457190, 17 Jun 2009. Huang, T. T., Kelley, A., Mclaughlin, J., Juan, T. T., Aaron, K., John, M., et al. (2010). Fermentation broth formulations. PCT Patent Applications WO2010096673, 26 Aug 2010. Huang, Y.-H., Lai, Y.-J., & Chou, C.-C. (2011). Fermentation temperature affects the antioxidant activity of the enzyme-ripened sufu, an oriental traditional fermented product of soybean. Journal of Bioscience and Bioengineering, 112(1), 49---53. Hyeon, J. E., You, S. K., Kang, D. H., Ryu, S.-H., Kim, M., Lee, S.-S., et al. (2014). Enzymatic degradation of lignocellulosic biomass by continuous process using laccase and cellulases with the aid of scaffoldin for ethanol production. Process Biochemistry, 49, 1266---1273. Iizuka-Furukawa, S., Isogai, A., Kusaka, K., Fujii, T., & Wakai, Y. (2017). Identification of 4-mercapto-4-methylpentan-2-one as the characteristic aroma of sake made from low-glutelin rice. Journal of Bioscience and Bioengineering, 123, 209---215. Inoue, Y., Kato, S., Saikusa, M., Suzuki, C., Otsubo, Y., Tanaka, Y., et al. (2016). Analysis of the cooked aroma and odorants that

17

contribute to umami soy miso (Japanese soybean paste). Food Chemistry, 213, 521---552. Irfan, M., Nadeem, M., & Syed, Q. (2014). One-factor-at-a-time (OFAT) optimization of xylanase production from Trichoderma viride-IR05 in solid-state fermentation. Journal of Radiation Research and Applied Sciences, 7, 317---326. Ito, T., Suzuki, N., Nakayama, A., Ito, M., & Hashizume, K. (2014). Factors affecting phenolic acid liberation from rice grains in the sake brewing process. Journal of Bioscience and Bioengineering, 118, 640---645. Jao, C.-L., Ko, W.-C., & Hsu, K.-C. (2011). Studies on the cooking conditions and mechanical koji making of black beans. Procedia Food Science, 1, 1388---1395. Jiang, P., Wang, Y., Jiang, J., & Zhu, Y. (2011). Method for producing cordyceps militaris fermentation rice by utilizing solid state fermentation of rice. Chinese Patent Application CN102172273, 07 Sep 2011. Joshi, C., Mathur, P., & Khare, S. K. (2011). Degradation of phorbol esters by Pseudomonas aeruginosa PseA during solid-state fermentation of deoiled Jatropha curcas seed cake. Bioresource Technology, 102, 4815---4819. Kapilan, R., & Arasaratnam, V. (2011). Paddy husk as support for solid state fermentation to produce xylanase from Bacillus pumilus. Rice Science, 18, 36---45. Kawauchi, M., & Iwashita, K. (2014). Functional analysis of histone deacetylase and its role in stress response drug resistance and solid-state cultivation in Aspergillus oryzae. Journal of Bioscience and Bioengineering, 118(2), 172---176. Karp, S. G., Faraco, V., Amore, A., Birolo, L., Giangrande, C., Soccol, V. T., et al. (2012). Characterization of laccase isoforms produced by Pleurotus ostreatus in solid state fermentation of sugarcane bagasse. Bioresource Technology, 114, 735---739. Kaur, S., Dhillon, G. S., Brar, S. K., & Chauhan, V. B. (2012). Carbohydrate degrading enzyme production by plant pathogenic mycelia and microsclerotia isolates of Macrophomina phaseolina through koji fermentation. Industrial Crops and Products, 36, 140---148. Kaushik, P., Mishra, A., & Malik, A. (2014). Dual application of agricultural residues for xylanase production and dye removal through solid state fermentation. International Biodeterioration & Biodegradation, 96, 1---8. Kholif, A. E., Elghandour, M. M. Y., Rodríguez, G. B., Olafadehan, O. A., & Salem, A. Z. M. (2016). Anaerobic ensiling of raw agricultural waste with a fibrolytic enzyme cocktail as a cleaner and sustainable biological product. Journal of Cleaner Production, http://dx.doi.org/10.1016/j.jclepro.2016.11.012 (in press) Kim, S. A., Yun, S. J., Jeon, S. H., Kim, N. H., Kim, H. W., Cho, T. J., et al. (2015). Microbial composition of turbid rice wine (Makgeolli) at different stages of production in a real processing line. Food Control, 53, 1---8. Kim, S. B., Liu, Y., & Zhang, L. (2016). Novel solid state fermentation device. Chinese Patent Application CN205099673, 23 Mar 2016. Koroleva, O. V., Gavrilova, V. P., Stepanova, E. V., Lebedeva, V. I., Sverdlova, N. I., Landesman, E. O., et al. (2002). Production of lignin modifying enzymes by co-cultivated white-rot fungi Cerrena maxima and Coriolus hirsutus and characterization of laccase from Cerrena maxima. Enzyme and Microbial Technology, 30, 573---580. Krogh, K., & Harris, P. (2007). Polypeptides having beta-glucosidase activity and polynucleotide encoding same. PCT Patent Application WO2007019442, 15 Feb 2007. Kuhad, R. C., Deswal, D., Sharma, S., Bhattacharya, A., Jain, K. K., Kaur, A., et al. (2016). Revisiting cellulase production and redefining current strategies based on major challenges. Renewable and Sustainable Energy Reviews, 55, 249---272. Kumar, M., Joshi, A., Kashyap, R., & Khanna, S. (2011). Production of xylanase by Promicromonospora sp MARS with rice straw under non sterile conditions. Process Biochemistry, 46, 1614---1618.

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

18 Lai, H., Xue, Q., & Yang, B. (2016). Microbial agent production line. Chinese Patent Application CN105349408, 24 Feb 2016. Lang, X., & Zhang, T. (2010). Automatic chain-type solid-state fermentation reaction device and method of automatic solid-state fermentation thereof. Chinese Patent Application CN101717716, 02 Jun 2010. Lenz, J., & Hölker, U. (2004). Trickle-film processing: An alternative for producing fungal enzymes. BioForum Europe, 6, 55---57. Li, J. (2009). Method for brewing vinegar by solid and liquid combination fermentation. Chinese Patent Application CN101451101, 10 Jun. 2009. Lim, B. G., Ng, T. L., Heyland, S., & Dac, T. H. (1999). Production of hydrolysate. PCT Patent Application WO9922608, 14 May 1999. Lim, J.-H., Jung, E.-S., Choi, E.-K., Jeong, D.-Y., Jo, S.-W., Jin, J.-H., et al. (2015). Supplementation with Aspergillus oryzae fermented kochujang lowers serum cholesterol in subjects with hyperlipidemia. Clinical Nutrition, 34, 383---387. Liu, D., Zhu, Y., Beeftink, R., Ooijkaas, L., Rinzema, A., Chen, J., et al. (2004). Chinese vinegar and its solid-state fermentation process. Food Reviews International, 20, 407---424. Liu, X., Wu, X., Yang, L., & Zhou, Q. (2009). Low-salt liquid state fermented soy sauce production process. Chinese Patent Application CN101595972, 09 Dec 2009. Liu, D., Zhang, R., Yang, X., Wu, H., Xu, D., Tang, Z., et al. (2011). Thermostable cellulase production of Aspergillus fumigatus Z5 under solid-state. International Biodeterioration & Biodegradation, 65, 717---725. Liu, Y., Li, C., Meng, X., & Yan, Y. (2016). Biodiesel synthesis directly catalyzed by the fermented solid of Burkholderia cenocepacia via solid state fermentation. Fuel Processing Technology, 106, 303---309. Liu, X., Song, J., Xia, T., Wang, M., Zhang, X., & Zheng, Y. (2016b). Health care vinegar and brewing process thereof. Chinese Patent Application CN105505732, 20 Apr 2016. Lombard, C. K. (2001). Process for the production of organic products from lignocellulose containing biomass sources. PCT Patent Application WO200132715, 10 May 2001. Luke, A. K., & Burton, S. G. (2001). A novel application for Neurospora crassa: Progress from batch culture to a membrane bioreactor for the bioremediation of phenols. Enzyme and Microbial Technology, 29(6---7), 348---356. Lv, X.-C., Cai, Q.-Q., Ke, X.-X., Chen, F., Rao, P.-F., & Ni, L. (2015). Characterization of fungal community and dynamics during the traditional brewing of Wuyi Hong Qu glutinous rice wine by means of multiple culture-independent methods. Food Control, 54, 231---239. Lv, X.-C., Huang, R.-L., Chen, F., Zhang, W., Rao, P.-F., & Ni, L. (2013). Bacterial community dynamics during the traditional brewing of Wuyi Hong Qu glutinous rice wine as determined by culture-independent methods. Food Control, 34, 300---306. Lueth, P., & Wismar, P. L. (2005). Solid state fermenter. European Patent EP1502946, 02 Feb 2005. Madrera, R. R., Bedrinana, R. P., & Valles, B. S. (2015). Production and characterization of aroma compounds from apple pomace by solid-state fermentation with selected yeasts. LWT --- Food Science and Technology, 64, 1342---1353. Maeda, Y., Okuda, M., Hashizume, K., Joyo, M., & Mikami, S. (2011). Analyses of peptides in sake mash: Forming a profile of bitter-tasting peptides. Journal of Bioscience and Bioengineering, 112(3), 238---246. Mai, H. T. N., Lee, K. M., & Choi, S. S. (2016). Enhanced oxalic acid production from corncob by a methanol-resistant strain of Aspergillus niger using semi solid-sate fermentation. Process Biochemistry, 51, 9---15. Martín-Sampedro, R., Eugenio, M. E., & Villar, J. C. (2012). Effect of steam explosion and enzymatic pre-treatments on pulping and bleaching of Hesperaloe funifera. Bioresource Technology, 111, 460---467.

C.R. Soccol et al. Martins, S., Mussatto, S. I., Martínez-Avila, G., Monta˜ nez-Saenz, J., Aguilar, C. N., & Teixeira, J. A. (2011). Bioactive phenolic compounds: Production and extraction by solid-state fermentation. A review. Biotechnology Advances, 29, 365---373. Marui, J., Tada, S., Fukuoka, M., Wagu, Y., Shiraishi, Y., & Kitamoto, N. (2013). Reduction of the degradation activity of umamienhancing purinic ribonucleotide supplement in miso by the targeted suppression of acid phosphatases in the Aspergillus oryzae starter culture. International Journal of Food Microbiology, 166, 238---243. Mathur, G., Mathur, A., Sharma, B. M., & Chauhan, R. S. (2013). Enhanced production of laccase from Coriolus sp. using PlackettBurman design. Journal of Pharmacy Research, 6, 151---154. Melikoglu, M., Lin, C. S. K., & Webb, C. (2013). Kinetic studies on the multi-enzyme solution produced via solid-state fermentation of waste bread by Aspergillus awamori. Biochemical Engineering Journal, 80, 76---82. Mendonc ¸a, R., Guerra, A., & Ferraz, A. (2002). Delignification of Pinus taeda wood chips treated with Ceriporiopsis subvermispora for preparing high-yield kraft pulps. Journal of Chemical Technology and Biotechnology, 77, 411---418. Meza, J. C., Auria, R., Lomascolo, A., Sigoillot, J.-C., & Casalot, L. (2007). Role of ethanol on growth, laccase production and protease activity in Pycnoporus cinnabarinus ss3. Enzyme and Microbial Technology, 41, 162---168. Moy, Y.-S., Lu, T.-J., & Chou, C.-C. (2012). Volatile components of the enzyme-ripened sufu, a Chinese traditional fermented product of soy bean. Journal of Bioscience and Bioengineering, 113(2), 196---201. Nagar, S., Mittal, A., Kumar, D., Kumar, L., Kuhad, R. C., & Gupta, V. K. (2011). Hyper production of alkali stable xylanase in lesser duration by Bacillus pumilus SV-85S using wheat bran under solid state fermentation. New Biotechnology, 28, 581---587. Ncube, T., Howard, R. L., Abotsi, E. K., Jansen van Rensburg, E. L., & Ncube, I. (2012). Jatropha curcas seed cake as substrate for production of xylanase and cellulase by Aspergillus niger FGSCA733 in solid-state fermentation. Industrial Crops and Products, 37, 118---123. OECD. (2009). Patent statistics manual (second edition). Organisation for Economic Co-operation and Development (OECD). Ohata, M., Uchida, S., Zhou, L., & Arihara, K. (2016). Antioxidant activity of fermented meat sauce and isolation of an associated antioxidant peptide. Food Chemistry, 194, 1034---1039. Okutsu, K., Yoshizaki, Y., Ikeda, N., Kusano, T., Hashimoto, F., & Takamine, K. (2015). Antioxidants in heat-processed koji and the production mechanisms. Food Chemistry, 187, 364---369. Okutsu, K., Yoshizaki, Y., Takamine, K., Tamaki, H., Ito, K., & Sameshima, Y. (2012). Development of a heat-processing method for koji to enhance its antioxidant activity. Journal of Bioscience and Bioengineering, 113(3), 349---354. Orozco, A. L., Pérez, M. I., Guevara, O., Rodríguez, J., Hernández, M., González-Vila, F. J., et al. (2008). Biotechnological enhancement of coffee pulp residues by solid-state fermentation with Streptomyces. Py---GC/MS analysis. Journal of Analytical and Applied Pyrolysis, 81, 247---252. Ozturkoglu-Budak, S., Wiebenga, A., Bron, P. A., & de Vries, R. P. (2016). Protease and lipase activities of fungal and bacterial strains derived froman artisanal raw ewe’s milk cheese. International Journal of Food Microbiology, 237, 17---27. Pandey, A. (2003). Solid-state fermentation. Biochemical Engineering Journal, 13, 81---84. Pandey, A. K., Edgard, G., & Negi, S. (2016). Optimization of concomitant production of cellulase and xylanase from Rhizopus oryzae SN5 through EVOP-factorial design technique and application in Sorghum Stover based bioethanol production. Renewable Energy, 98, 51---56. Panwar, D., Srivastava, P. K., & Kapoor, M. (2014). Production, extraction and characterization of alkaline xylanase from

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

Recent developments and innovations in solid state fermentation Bacillus sp. PKD-9 with potential for poultry feed. Biocatalysis and Agricultural Biotechnology, 3, 118---125. Pirota, R. D. P. B., Tonelotto, M., Delabona, P. S., Fonseca, R. F., Paixão, D. A. A., Baleeiro, F. C. F., et al. (2013). Enhancing xylanases production by a new Amazon Forest strain of Aspergillus oryzae using solid-state fermentation under controlled operation conditions. Industrial Crops and Products, 45, 465---471. Qureshi, A. S., Khushk, I., Ali, C. H., Chisti, Y., Ahmad, A., & Majeed, H. (2016). Coproduction of protease and amylase by thermophilic Bacillus sp. BBXS-2 using open solid-state fermentation of lignocellulosic biomass. Biocatalysis and Agricultural Biotechnology, 8, 146---151. Raimbault, M., & Germon, J. C. (1976). Procédé d’enrichissement en protéines de produits comestibles solides, French Patent No. 76-06-677. Rastogi, S., Soni, R., Kaur, J., & Soni, S. K. (2016). Unravelling the capability of Pyrenophora phaeocomes S-1 for the production of ligno-hemicellulolytic enzyme cocktail and simultaneous bio-delignification of rice straw for enhanced enzymatic saccharification. Bioresource Technology, 222, 458---469. Ravikumar, G., Gomathi, D., Kalaiselvi, M., & Uma, C. (2012). A protease from the medicinal mushroom Pleurotus sajorcaju: Production, purification and partial characterization. Asian Pacific Journal of Tropical Biomedicine, S411---S417. Riker Laboratories Inc. (1962). Production of pyrogen-free penicillinase. British Patent GB887408, 17 Jan 1962. Rodríguez-Couto, S., & Toca-Herrera, J. L. (2006). Industrial and biotechnological applications of laccases: A review. Biotechnology Advances, 24(5), 500---513. Rodríguez-Fernández, D. E., Rodríguez-León, J. A., Carvalho, J. C., Sturm, W., & Soccol, C. R. (2011). The behavior of kinetic parameters in production of pectinase and xylanase by solid-state fermentation. Bioresource Technology, 102, 10657---10662. Ropars, J., de la Vega, R. C. R., López-Villavicencio, M., Gouzy, J., Sallet, E., Dumas, E., et al. (2015). Adaptive horizontal gene transfers between multiple cheese-associated fungi. Current Biology, 25, 2562---2569. Sahnoun, M., Kriaa, M., Elgharbi, F., Ayadi, D.-Z., Bejar, S., & Kammoun, R. (2015). Aspergillus oryzae S2 alpha-amylase production under solid state fermentation: Optimization of culture conditions. International Journal of Biological Macromolecules, 75, 73---80. Salar, R. K., Purewal, S. S., & Bhatti, M. S. (2016). Optimization of extraction conditions and enhancement of phenolic content and antioxidant activity of pearl millet fermented with Aspergillus awamori MTCC-548. Resource-Efficient Technologies, 2, 148---157. Sethi, B. K., Jana, A., Nanda, P. K., Mohapatrac, P. K. D., & Sahoo, S. L. (2016). Thermostable acidic protease production in Aspergillus terreus NCFT 4269.10 using chickling vetch peels. Journal of Taibah University for Science, 10, 571---583. Sicard, M., Baudrit, C., Leclerc-Perlat, M. N., Wuillemin, P. H., & Perrot, N. (2011). Expert knowledge integration to model complex food processes. Application on the Camembert cheese ripening process. Expert Systems with Applications, 38, 11804---11812. Sicard, M., Perrot, N., Reuillon, R., Mesmoudi, S., Alvarez, I., & Martin, S. (2012). A viability approach to control food processes: Application to a Camembert cheese ripening process. Food Control, 23, 312---319. Singh, S., & Gupta, A. (2014). Comparative fermentation studies on amylase production by Aspergillus flavus TF-8 using Sal (Shorea robusta) deoiled cake as natural substrate: Characterization for potential application in detergency. Industrial Crops and Products, 57, 158---165. Singh, M. K., Singh, J., Kumar, M., & Thakur, I. S. (2014). Novel lipase from basidiomycetes Schizophyllum commune ISTL04, produced

19

by solid state fermentation of Leucaena leucocephala seeds. Journal of Molecular Catalysis B: Enzymatic, 110, 92---99. Singhania, R. R., Patel, A. K., Soccol, C. R., & Pandey, A. (2009). Recent advances in solid-state fermentation. Biochemical Engineering Journal, 44, 13---18. Sobol, C. V., & Sobol, Y. T. (2003). Composition and method for producing and use of a fermented hydrolyzed medium containing microorganisms and products of their metabolism. US Patent Application US2003235559, 25 Dec 2003. Spier, M. R., Vandenberghe, L. P. S., Medeiros, A. B. P., & Soccol, C. R. (2011). Application of different types of bioreactors in bioprocesses. In P. G. Antolli, & Z. Liu (Eds.), Bioreactors: Design, properties and applications (pp. 53---88). New York: Nova Science Publishers. Soccol, C. R., & Vandenberghe, L. P. S. (2003). Overview of solidstate fermentation in Brazil. Biochemical Engineering Journal, 13, 205---218. Sun, B. (2007). Cereals nutrient wine and its production. Chinese Patent Application CN1982430, 20 Jun 2007. Suzuki, N., Ito, T., Hiroshima, K., Tokiwano, T., & Hashizume, K. (2016). Formation of ethyl ferulate from feruloylated oligosaccharide by transesterification of rice koji enzyme under sake mash conditions. Journal of Bioscience and Bioengineering, 121(3), 281---285. Suryanarayan, S., Mazumdar, K., & Mazumdar, K. C. (2000). Solid state fermentation. PCT Patent Application WO200029544, 25 May 2000. Srianta, I., Zubaidah, E., Estiasih, T., Yamada, M., & Harijono. (2016). Comparison of Monascus purpureus growth, pigment production and composition on different cereal substrates with solid state fermentation. Biocatalysis and Agricultural Biotechnology, 7, 181---186. Takashita, H., Fujihara, E., furutera, M., Kajiwara, Y., Shimoda, M. M., Ogawa, T., et al. (2013). Competitive advantage and tolerance of selected shochu yeast in barley shochu mash. Journal of Bioscience and Bioengineering, 116(1), 79---84. Tanaka, Y., Watanabe, J., & Mogi, Y. (2012). Monitoring of the microbial communities involved in the soy sauce manufacturing process by PCR-denaturing gradient gel electrophoresis. Food Microbiology, 31, 100---106. Thanapimmetha, A., Luadsongkram, A., Titapiwatanakun, B., & Srinophakun, P. (2012). Value added waste of Jatropha curcas residue: Optimization of protease production in solid state fermentation by Taguchi DOE methodology. Industrial Crops and Products, 37, 1---5. Thomas, L., Larroche, C., & Pandey, A. (2013). Current developments in solid-state fermentation. Biochemical Engineering Journal, 81, 146---161. Trontel, A., Batu, A., Gusi, I., Slavica, A., Santek, B., & Novak, S. (2011). Production of d- and l-lactic acid by mono- and mixed cultures of Lactobacillus sp. Food Technology and Biotechnology, 49, 75---82. Veerabhadrappa, M. B., Shivakumar, S. B., & Devappa, S. (2014). Solid-state fermentation of Jatropha seed cake for optimization of lipase, protease and detoxification of anti-nutrients in Jatropha seed cake using Aspergillus versicolor CJS-98. Journal of Bioscience and Bioengineering, 117, 208---214. Velmurugan, P., Hur, H., Balachandar, V., Kamala-Kannan, S., Lee, K. J., Lee, S. M., et al. (2011). Monascus pigment production by solid-state fermentation with corn cob substrate. Journal of Bioscience and Bioengineering, 112, 590---594. Vlasenko, E., Cherry, J., & Xu, F. (2005). Methods for degrading lignocellulosic materials. US Patent Application US2005164355, 28 Jul. 2005. Voigt, D. D., Patterson, M. F., Linton, M., & Kelly, A. L. (2011). Effect of high-pressure treatment of milk prior to manufacture on ripening of Camembert cheese. Innovative Food Science and Emerging Technologies, 12, 1---5.

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002

+Model BIORI-2; No. of Pages 20

ARTICLE IN PRESS

20 Wang, F., Gao, B., & Yao, R. (2006). Cluster sprinkling fermentation method for preparing fruit vinegar in liquid and solid states and fermentation equipment. Chinese Patent Application CN1661001, 31 Aug 2006. Watanabe, J., Tanaka, H., Mogi, Y., Yamazaki, T., Suzuki, K., Watanabe, T., et al. (2011). Loss of Aspergillus oryzae amyR function indirectly affects hemicellulolytic and cellulolytic enzyme production. Journal of Bioscience and Bioengineering, 11(4), 408---413. Wei, X. (2001). A milestone of condiments administration with industrial standard. Chinese Condiment, 1, 3---8. Wei, C.-L., Chao, S.-H., Tsai, W.-B., Lee, P.-S., Tsau, N.-H., Chen, J.-S., et al. (2013). Analysis of bacterial diversity during the fermentation of inyu, a high-temperature fermented soy sauce, using nested PCR-denaturing gradient gel electrophoresis and the plate count method. Food Microbiology, 33, 252---261. WIPO. (2016). International Patent Classification Version 2016: Guide to the IPC. WTO. (1994). Agreement on Trade-Related Aspects of Intellectual Property Rights (TRIPS). Marrakesh: World Trade Organization (WTO). Yamada, O., Takara, R., Hamada, R., Hayashi, R., Tsukahara, M., & Mikami, S. (2011). Molecular biological researches of Kuro-Koji molds, their classification and safety. Journal of Bioscience and Bioengineering, 112(3), 233---237. Yan, Y.-Z., Qian, Y.-L., Ji, F.-D., Chen, J.-Y., & Han, B.-Z. (2013). Microbial composition during Chinese soy sauce koji-making based on culture dependent and independent methods. Food Microbiology, 34, 189---195.

C.R. Soccol et al. Yazid, N. A., Barrena, R., & Sánchez, A. (2016). Assessment of protease activity in hydrolysed extracts from SSF of hair waste by and indigenous consortium of microorganisms. Waste Management, 49, 420---426. Yong, X., Raza, W., Yu, G., Ran, W., Shen, Q., & Yang, X. (2011). Optimization of the production of poly-gamma-glutamic acid by Bacillus amyloliquefaciens C1 in solid-state fermentation using dairy manure compost and monosodium glutamate production residues as basic substrates. Bioresource Technology, 102, 7548---7554. Yoon, L. W., Ang, T. N., Ngoh, G. C., & Chua, A. S. M. (2014). Fungal solid-state fermentation and various methods of enhancement in cellulase production. Biomass and Bioenergy, 67, 319---338. Yu, J. (2011). Soy sauce without preservative. Chinese Patent Application CN102090614, 15 Jun 2011. Zhang, B., Guan, Z.-B., Cao, Y., Xie, G.-F., & Lu, J. (2015). Secretome of Aspergillus oryzae in Shaoxing rice wine koji. International Journal of Food Microbiology, 155, 113---119. Zhang, L., Zhang, H., Wang, Z., Chen, G., & Wang, L. (2016). Dynamic changes of the dominant functioning microbial community in the compost of a 90-m3 aerobic solid state fermentor revealed by integrated meta-omics. Bioresource Technology, 203, 1---10. Zheng, X. W., Yan, Z., Nout, M. J. R., Smid, E. J. S., Zwietering, M. H., Boekhout, T., et al. (2014). Microbiota dynamics related to environmental conditions during the fermentative production of Fen-Daqu, a Chinese industrial fermentation starter. International Journal of Food Microbiology, 182---183, 57---62. Zhu, Y., & Tramper, J. (2013). Koji --- Where East meets West in fermentation. Biotechnology Advances, 31, 1448---1457.

Please cite this article in press as: Soccol, C. R., et al. Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation (2017), http://dx.doi.org/10.1016/j.biori.2017.01.002